Review of the Distribution of the Family Gobiidae (Pisces)

ECOLOGIA BALKANICA
2013, Vol. 5, Issue 2
December 2013
pp. 81-89
Review of the Distribution of the Family Gobiidae (Pisces)
in the Bulgarian Danube Tributaries
Velislav Y. Zarev*, Apostolos I. Apostolou,
Boris K. Velkov, Milen V. Vassilev†
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences
2 Gagarin Street, 1113 Sofia, BULGARIA
*Corresponding author: [email protected]
Abstract. The current study aims to give in detailed information on the actual distribution of the
species from family Gobiidae in the Bulgarian Danube tributaries. All known literature has been
revised and with the new data collected is given complete and actual information on their
distribution. In the period 2010-2012 were sampled a total of 41 sites alongside each one of the
Bulgarian Danube tributaries. The sampling started from the river mouths to upstream in order to
discover what is the southern (upstream) distribution of each one goby species. Four goby species
were recorded from the tributaries – the round goby (Neogobius melanostomus Pallas, 1814), the
monkey goby (Neogobius fluviatilis), the racer goby (Neogobius gymnotrachelus) and the tubenose
goby (Proterorhinus marmoratus). Further analysis showed preference of mixed substrates and silt in
addition of homogenous ones. The occurrence of gobies in the studied tributaries decreased
inversely proportional to distance from Danube.
Key words: freshwater gobies, distribution, invasive species, family Gobiidae, the Danube River
tributaries
Introduction
The Danube River is the second longest
river in Europe with length of 2850 km. Its
springs are located in Germany. It flows
through 10 countries, having more than 300
tributaries and mouths into the Black Sea.
The Bulgarian sector of the Danube River is
located between 845 and 375 river
kilometers and is typical low river stretch.
The major tributaries in Bulgarian sector are
12 (Fig. 1).
The saprobic characteristics of the
different Bulgarian Danube tributaries in
their middle and low sections vary between
alpha to I or II beta-mesosaprobic conditions
(RUSEV, 1994). The main factors that
influence the saprobic index are the season,
© Ecologia Balkanica
http://eb.bio.uni-plovdiv.bg
proximity to cities and villages, industrial
and agricultural pollution.
Danube is one of the water bodies with
highest
biodiversity
and
ecological
significance in Europe. The main reasons for
this are the huge water flow, diverse
ecological conditions and the geographical
location (BĂNĂRESCU, 1964).The ichthyofauna of the Bulgarian sector of the Danube
consists of 68 species (VASSILEV &
PEHLIVANOV, 2005) and it is heterogeneous –
consists of native pre-Pleistocene fish forms
and post-glacial immigrants (BĂNĂRESCU,
1991).
The distribution of the freshwater
gobies along the Danube is relatively well
known, as the first researches on the topic
Union of Scientists in Bulgaria – Plovdiv
University of Plovdiv Publishing House
Review of the Distribution of the Family Gobiidae (Pisces) in the Bulgarian Danube Tributaries
for the Bulgarian section of the river have
been done in the beginning of the XX
century.
DRENSKY (1948, 1951) reported for the
presence of the stellate tadpole goby
(Benthophilus stellatus Sauvage, 1874) in the
Bulgarian parts of the Danube – near the
towns of Svishtov and Nikopol.
The monkey goby (Neogobius fluviatilis
Pallas, 1814) was recorded for the first time
in the Bulgarian Danube by DRENSKY (1921).
Later the author confirmed the presence of
the species in Danube (DRENSKY, 1948,
1951).
DRENSKY (1948, 1951) found the racer
goby (Neogobius gymnotrachelus Kessler,
1857) in the Danube up to Ruse. Later
GHEORGHIEV (1966) reported that the racer
goby can be found up to Vidin.
The Kessler’s goby (Neogobius kessleri
Günther, 1861) was found in the past in the
Danube up to the city of Vidin (DRENSKY,
1921, 1948, 1951), as the same author also
stated that he got evidence for the presence
of the species up to the city of Vienna.
The natural distribution of the round
goby (Neogobius melanostomus Pallas, 1814)
covered the lower sections of Danube River
upstream to the town of Vidin (DRENSKY,
1948, 1951).
In the Danube the presence of the
tubenose goby (Proterorhinus marmoratus
Pallas, 1814) was registered by DRENSKY
(1948). He stated that the species can be
found upstream to Bratislava (1869 river
km). Later GHEORGHIEV (1966) discovered
the tubenose goby near the cities of Ruse,
Svishtov and Vidin.
MARINOV (1966) reported the presence
of 5 species of gobies in the Danube - N.
kessleri, N. fluviatilis, Pr. marmoratus, B.
stellatus
and
mis-determinated
and
currently not present in the Danube
Neogobius cephalarges constructor Nordmann,
1840.
According to the latest data (VASSILEV
& PEHLIVANOV, 2005; POLAČIK et al., 2008;
VASSILEV et al., 2011) family Gobiidae in the
Bulgarian sector of Danube is represented
by three genera with six species: stellate
tadpole goby, monkey goby, racer goby,
Kessler’s goby, round goby and tubenose
goby. All of them are Ponto-Caspian relicts
and are native in the Bulgarian section of the
Danube. Recently there are clear indications
for fast invasion of some of the gobies
upstream (HEGEDIŠ et al., 1991; KAUTMAN,
2001; GUTI, 2004; PRASEK & JURAJDA, 2005;
WEISNER, 2005; MANNÉ & POULET, 2008;
POLAČIK et al., 2009).
The ichthyofaunistic studies of the
Bulgarian Danube tributaries showed
presence of gobies mainly in the lower
sections of the rivers and in the rivermouths.
KARAPETKOVA (1985) reported the
occurrence of B. stellatus in the Ogosta River,
but only close to the river mouth in to the
Danube.
According to DRENSKY (1932) N.
fluviatilis was captured in lower and mid
sections of the Osam River. Later DRENSKY
(1948) discovered the monkey goby in the
rivers Iskar, Osam, Yantra and Vit (up to
Pleven, 41 km form Danube). DRENSKY
(1951) found the species in Ogosta River.
KARAPETKOVA (1985) report for the presence
of N. fluviatilis in the Iskar, Ogosta, Vit,
Rusenski Lom River, and in the Tsibritsa
River near the village of Zlatiya (5 km from
Danube). Later the species was reconfirmed
for the Rusenski Lom River complex (MIHOV
& KOEV, 2006). PEHLIVANOV et al. (2009)
stated the presence of N. fluviatilis in the Vit
River. According to another recent study
(TRICHKOVA et al., 2009) the monkey goby
can be found in the rivers Vidbol (lower
reaches), the Archar (Archar village), the
Ogosta (near Mizia) and the Lom River (near
Lom). The species is reconfirmed for the
Yantra River (VASSILEV et al. 2009).
KARAPETKOVA & DIKOV (1986) reported
for the presence of the racer goby in Vit
River, after two years it was found also in
the
Rusenski
Lom
River
complex
(KARAPETKOVA & UNDZIAN, 1988). VASSILEV
et al. (2009) confirmed the presence of the N.
gymnotrachelus in Yantra River up to Polsko
Kosovo village (52 km from Danube).
The Kessler’s goby was registered in the
lower sections of the Osam River by
DRENSKY (1932) and in the Vit River by
GHEORGHIEV (1966). KARAPETKOVA (1985)
reported for the presence of the N. kessleri in
82
Velislav Y. Zarev, Apostolos I. Apostolou, Boris K. Velkov, Milen V. Vassilev†
Ogosta. Some authors assume that in the
past it reached upstream to the Iron Gates
Dam (943 river km) in Serbia (BĂNĂRESCU,
1970, MILLER, 2003).
DRENSKY (1948) reported for the
presence of the round goby in the Vit River
up to Pleven (41 km from the Danube).
Later the species was caught in the Iskar
River (KARAPETKOVA, 1985). TRICHKOVA et
al. (2009) found N. melanostomus in the
Archar (close to Archar village) and the
Ogosta River (found near Mizia village).
The species was also found in the Yantra
River (VASSILEV et al. 2009).
KARAPETKOVA (1985) reported for the
presence of the Pr. marmoratus in the Ogosta
River. The tubenose goby was registered for
the Archar, Vidbol, and Skat (found near
Galitsche village) and in the Ogosta River
was confirmed for two locations – near
Mihailovo village and near Hayredin village
(TRICHKOVA et al., 2009). Tubenose goby was
registered for the Yantra River by Vassilev
(VASSILEV et al. 2009).
Materials and Methods
The ichthyofaunistic survey was carried
out during March, 2010 – April, 2012. A total
of 41 sites were sampled alongside each one
of the Bulgarian Danube tributaries (Fig. 1,
Table 1, 2).
Fig. 1. Map of the Bulgarian Danube tributaries with the sampling sites. In the presented
map the Danube River is water border between Bulgaria and Romania. The numbers
correspond to the rivers as follow: 1 – Voynishka, 2 – Vidbol, 3 – Archar, 4 – Lom, 5 –
Tsibritsa, 6 – Ogosta, 7 – Skat, 8 – Iskar, 9 – Vit, 10 – Osam, 11 – Yantra, 12 – Rusenski Lom
River complex.
Two rivers were excluded of the
sampling – the heavily polluted, water
border with Serbia – Timok River and the
Topolovitsa River, which has low water
flow and is heavily vegetated and canalized.
The sampling in each tributary started from
the river mouth and continues upstream in
order to give actual information about the
southern distribution of the gobies in these
rivers. Fishes were captured by standard
portable electrofishing device. A transect of
100 m was sampled at each site, as if there
were some obstacles in the river course we
sampled the river section below and above
them in order to complete the transect. Seine
nets were used for sampling in the Ogosta
Reservoir. The applied sampling methods
have been focused on capturing gobies.
83
Review of the Distribution of the Family Gobiidae (Pisces) in the Bulgarian Danube Tributaries
Almost all fish species were identified in situ
and released back. Some of the captured
specimens were preserved in 95% ethanol
for further analyses. The percentages of
occurrence on both the given substrate and
given distance from Danube on the basis of
the whole occurrences of each species on all
registered substrate types and distances
from Danube respectively, have been
calculated.
Table 1. Sampling sites coordinates and recorded gobies for the period 2009 – 2012.The
following abbreviations were used: Nf – Neogobius fluviatilis, Ng – Neogobius gymnotrachelus,
Nm – Neogobius melanostomus, Pm – Proterorhinus marmoratus.
84
Velislav Y. Zarev, Apostolos I. Apostolou, Boris K. Velkov, Milen V. Vassilev†
Results
Four goby species from two genera
were recorded from the studied sites – N.
fluviatilis, N. gymnotrachelus, N. melanostomus
and Pr. marmoratus (Tab. 2). In the most
western studied rivers – the Voynishka and
the Vidbol River we did not found any goby
species. In the Archar River the presence of
two species was registered – N.
gymnotrachelus and Pr. marmoratus. In the
Lom River we found only Pr. marmoratus.
Two sites were sampled along the Tsibritsa
River and in the closest to the river mouthsampling site we found N. fluviatilis. In the
Ogosta River we sampled 5 sites and we
found gobies (N. fluviatilis, N. melanostomus
and Pr. marmoratus) in only three of them.
We also sampled in the Ogosta Reservoir,
which is located further upstream, and we
confirmed the presence of the N. fluviatilis in
it. In the Skat River we found only Pr.
marmoratus. In the longest river in Bulgaria –
Iskar we sampled 8 sites and registered the
presence of two goby species – N. fluviatilis
and N. melanostomus. In the Vit River we
recorded the presence of three goby species
– N. fluviatilis, N. gymnotrachelus and N.
melanostomus. In the Osam River we took
samples from two locations but did not
found any gobies. For the Yantra River we
compared our data (Table 2) with a previous
study on the ichthyofauna of this river
(VASSILEV et al., 2009), and did not found
any changes. In the Rusenski Lom River
complex we sampled 7 locations (Fig. 1,
Table 2). We registered the presence of the
monkey goby in 4 of them – up to the
Ivanovo village (42 km from the Danube).
The
calculated
percentages
of
occurrence of the registered gobiid species
on a given substrate on the basis of all types
of substrates where the species is discovered
showed that all of them prefer mixed
substrates or the border between different
substrates, rather than one type of substrate
(Fig. 2). A deviation has been established for
silt bottoms, where the percentage of
occurrence for three species is rather higher
than on gravel, sand or rock.
From the other side, as distance increases
upstream from the Danube River, the
occurrence of gobies decreases respectively
(Fig. 3). There is a gap between 70 and 80 km
from the Danube, where gobies have not
been established. The registrations between
85 and 100 km have been accomplished in
the Iskar and the Yantra Rivers.
Table 2. Distribution of the gobies in the
Bulgarian Danube tributaries.
River
Voynishka
Vidbol
Archar
Lom
Tsibritsa
Ogosta
and
Ogosta
Reservoir
Skat
Iskar
Vit
Osam
Yantra
Rusenski
Lom
Goby species
Additional
Ng Nf Nm Pm species
X
X
X
X
X
X
X
X
X
X
X
X
Bs, Nk
X
X
X
X
X
X
X
X
X
X
X
X
X
Nk
Nk
The following abbreviations were used:
Bs – Benthophilus stellatus, Nf – Neogobius
fluviatilis, Ng – Neogobius gymnotrachelus, Nk
– Neogobius kessleri, Nm – Neogobius
melanostomus,
Pm
–
Proterorhinus
marmoratus.
Discussion
The species inhabiting the tributaries of
the Danube River are determined in general
by the Danubian fish fauna, which is the
most abundant ichthyocomplex in Europe
consisting of more than 100 species
(BĂNĂRESCU, 1964) and 136 species for the
Danube delta. The gobies inhabiting the
Danube are freshwater or euryhaline,
autochthonous Ponto-Caspian relicts. Their
distribution is relatively well known and all
the available literature on this topic was
studied.
For the Yantra River we also
summarized the data from KARAPETKOVA
(1972) and VASSILEV et al. (2009).
85
Review of the Distribution of the Family Gobiidae (Pisces) in the Bulgarian Danube Tributaries
Fig. 2. Occurrence of the four discovered gobiid species in relation to the type of the
substrate, where each given species is registered. On the y axis is illustrated the percentage of
occurrence in given substrate, on the basis of the total number of occurrences.
Fig. 3. Occurrence of the four discovered gobiid species in relation to the upstream distance
from the Danube River, where each given species is registered. On the y axis is illustrated the
percentage of occurrence in given distance, on the basis of the total number of occurrences.
KARAPETKOVA (1972) reports for the
presence of N. fluviatilis and N. kessleri,
while VASSILEV et al. (2009) found all four
(N. gymnotrachelus, N. fluviatilis, N.
melanostomus, Pr. marmoratus) gobies in
different locations along the river (Table 2).
The southern points in these tributaries,
in which we registered the presence of goby
species, were in the Iskar River – 85 km
upstream from the Danube (125 m a.s.l.) and
in the Yantra River – 100 km from the
Danube (44 m a.s.l.).
The calculation of percentages of
occurrence on given substrate based on all
substrates where given species registered
showed preference for mixed substrates,
rather than homogenous, with exception of
silt bottoms. It is obvious that a more
heterogeneous bottom discloses more
opportunities for hiding/escaping from
predators and finding food items. A rather
86
Velislav Y. Zarev, Apostolos I. Apostolou, Boris K. Velkov, Milen V. Vassilev†
increased occurrence of three species on silt
is not surprising-in such substrates are
mostly appropriate for small benthic
invertebrates on which the gobies prey, but
do not give protection to gobies.
From the other side as distance from
Danube decreases, the occurrence of gobies
in the Danube tributaries decreases. This
happens earlier in smaller rivers (Tsibritsa,
Lom, Russenski Lom), in addition to the
bigger Danube tributaries (the Iskar and the
Yantra). The gobiid presence in the Ogosta
reservoir should be considered as an
isolated case; most probably N. fluviatilis
have been introduced by accident in this
particular water body.
Three of the studied gobies (N.
fluviatilis, N. kessleri and Pr. marmoratus) are
included in the IUCN Red List of threatened
species with the status Least concern (LC)
which indicates that they are not directly
endangered. They are also included in the
annex III (Protected fauna species) of the
Bern Convention – “Convention on the
conservation of European wildlife and
natural habitats” which includes species
that are in need of protection but can be
hunted or exploited with regulations.
Meanwhile these species are considered
invasive,
expanding
their
natural
distribution rapidly and colonizing new
territories far away from their native range.
In the past when the industry in
Bulgaria was highly developed, the saprobic
index of the rivers was worst. Now when
most of the factories are not operational the
saprobic index shows better values. This can
be one of the reasons for the observed recent
spreading of the gobies upstream in the
tributaries – the ecological conditions are
better and many of the pollutants are no
longer present in the water.
There is also fast expansion upstream
the Danube of the gobies recorded in the
last two decades. The reasons for this are
not still clarified. Some authors report that
the global climate change can influence the
invasion success (HARKA & BÍRÓ, 2007;
KORNIS et al., 2012), other the increased
transportation and unregulated release of
ballast waters (SAPOTA & SKÓRA, 2005;
BROWN & STEPIEN, 2008; HAYDEN & MINER,
2009), some the changed environmental
condition in the rivers and canalization
(HARKA & BÍRÓ, 2007) and last but not least
reason is given to the natural dispersion and
migration capabilities of this species (WOLFE
& MARSDEN, 1998; BRONNENHUBER et al.,
2011). Most probably, it is a combination of
all these factors.
From their widespread distribution and
recent invasions in new territories we can
assume that in Bulgaria they are not in an
urgent need of protection, as they are not
endangered, but are very important part of
the aquatic ecosystems in the Bulgarian
Danube tributaries and lakes alongside the
Danube like the world renowned Srebarna
Biosphere Reserve (PEHLIVANOV, 2000) and
are
important
study
object
for
understanding the ecology of the invasive
species and the reasons that leads up to this.
Acknowledgments
This work was prepared during the
project DO-02-201 “Black sea gobies –
biological resource with unvalued economic
significance”
2009-2012
financed
by
Bulgarian Science Fund in Ministry of
Education, Youth and Science.
†Associate prof. Dr. Milen Vassilev
suddenly passed away on 30.05.2013. He left
the article and much of his work
uncompleted. His colleagues will continue
his efforts.
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Received: 10.11.2013
Accepted: 20.12.2013
Union of Scientists in Bulgaria – Plovdiv
University of Plovdiv Publishing House